Strategies for Introducing Outpatient Specialty Palliative Care in Gynecologic Oncology

Abstract

Purpose:

Concern that patients will react negatively to the idea of palliative care is cited as a barrier to timely referral. Strategies to successfully introduce specialty palliative care to patients have not been well described. We sought to understand how gynecologic oncologists introduce outpatient specialty palliative care.

Methods:

We conducted a national qualitative interview study at six geographically diverse academic cancer centers with well-established palliative care clinics between September 2015 and March 2016. Thirty-four gynecologic oncologists participated in semistructured telephone interviews focusing on attitudes, experiences, and practices related to outpatient palliative care. A multidisciplinary team analyzed interview transcripts using constant comparative methods to inductively develop and refine a coding framework. This analysis focuses on practices for introducing palliative care.

Results:

Mean participant age was 47 years (standard deviation, 10 years). Mean interview length was 25 minutes (standard deviation, 7 minutes). Gynecologic oncologists described the following three main strategies for introducing outpatient specialty palliative care: focus initial palliative care referral on symptom management to dissociate palliative care from end-of-life care and facilitate early relationship building with palliative care clinicians; use a strong physician-patient relationship and patient trust to increase acceptance of referral; and explain and normalize palliative care referral to address negative associations and decrease patient fear of abandonment. These strategies aim to decrease negative patient associations and encourage acceptance of early referral to palliative care specialists.

Conclusion:

Gynecologic oncologists have developed strategies for introducing palliative care services to alleviate patient concerns. These strategies provide groundwork for developing system-wide best practice approaches to the presentation of palliative care referral.

INTRODUCTION

Early integration of specialty palliative care into standard oncology care is promoted by national organizations, including ASCO, the National Comprehensive Cancer Network, and the Society of Gynecologic Oncology.^1-3 Specialty palliative care improves quality of life and may increase survival among patients with advanced cancer.^4-9 Timely palliative care referral is essential in providing quality cancer care.

Despite its proven benefits, palliative care in oncology is still often delivered late in the disease course.^10,11 Oncologist concern that patients will react negatively to the idea of palliative care has been frequently identified as a barrier to timely referral.^12-17 This early barrier of patient decline of referral can severely limit the benefits reaped from integrated palliative care. As a result, understanding how oncologists effectively approach and address this concern would provide groundwork to guide future oncologist education and improve the integration of palliative care into standard oncology care.

We sought to understand how gynecologic oncologists introduce outpatient specialty palliative care and identify strategies used to facilitate patient acceptance of referral. We chose to examine the use of outpatient palliative care because outpatient referrals occur earlier in the disease course than inpatient consultations¹⁰ and are thus most concordant with recommendations for early palliative care referral.

METHODS

Study Design

We conducted a qualitative, in-depth interview study to understand gynecologic oncologists’ views on outpatient specialty palliative care. This study was approved by the University of Pittsburgh Institutional Review Board (PRO15070206). Results from this study have been previously published¹⁸; however, no prior analysis has examined the strategies gynecologic oncologists use to present palliative care to their patients.

Recruitment

Gynecologic oncologists at six National Cancer Institute–designated cancer centers with well-established outpatient palliative care clinics were approached for participation. Initial contact was by e-mail with follow-up to schedule interviews conducted via a combination of e-mail and direct contact by local colleagues. Institutions were selected from across the United States to ensure diversity of geography, gynecologic oncology program size, and palliative care clinic structure (Table 1). Eligible participants were attending-level, fellowship-trained gynecologic oncologists with an outpatient clinical practice of at least 1 half-day per week. Study authors were excluded from participation.

Table 1.

Institution Characteristics

Interviews

Semistructured, in-depth interviews were conducted via phone by a single study investigator trained in semistructured interviewing techniques (C.M.H.). Interviews occurred between September 2015 and March 2016. The study was approved by the University of Pittsburgh Institutional Review Board, and all participants provided verbal informed consent. Standard in-depth interviewing techniques focused on oncologist experiences and practices surrounding referral to outpatient specialty palliative care. Questions were designed to be open-ended and nonleading, and follow-up probes were used to elicit rich description of individual experiences. The interviewer was trained to pose questions in a neutral and nondirective manner. Questions elicited reflection on real patients and also presented brief vignettes involving hypothetical patients. The full interview guide is available in the Data Supplement.

Analysis

Audio recordings of interviews were transcribed verbatim. Line-by-line coding of a subset of transcripts facilitated inductive development of an initial coding framework. This technique, known as qualitative description, describes events or phenomena and the meanings attributed to these by participants.¹⁹ Concepts and codes were discussed, compared, and refined using constant comparative methodology²⁰ by a multidisciplinary team with expertise in palliative care, gynecologic oncology, qualitative research methodology, advanced practice nursing, anthropology, and public health. Emerging codes were iteratively applied to transcripts as they were obtained, with team discussion until agreement was reached on a final coding framework. The final coding framework was applied to all transcripts by a trained investigator (C.M.H.), and a second investigator (S.L.C.) coded 50% of the interviews, with comparison undertaken to ensure intercoder agreement. Disagreements were discussed and resolved by team consensus. Codes were classified, grouped, and refined into themes through an iterative, analytic process.¹⁹ ATLAS.ti Software (V 5.5.9; Scientific Software Development, Berlin, Germany) facilitated data analysis.

RESULTS

Thirty-four of 35 eligible gynecologic oncologists at six different institutions participated, for a response rate of 97%. One physician was unable to participate because of scheduling conflicts. Participants were gynecologic oncology board certified or eligible. One participant was board certified in palliative care, and no participants had completed a palliative care fellowship. Table 2 lists clinician characteristics. Average interview length was 25 minutes (standard deviation, 7 minutes; range, 14 to 45 minutes).

Table 2.

Participant Characteristics

In analysis of participant interviews, the following three themes emerged related to strategies gynecologic oncologists used to introduce outpatient specialty palliative care to their patients: focus initial palliative care referral on symptom management to dissociate palliative care from end-of-life care and facilitate early relationship building with palliative care clinicians; use a strong oncologist-patient relationship and patient trust to increase acceptance of referral; and normalize and explain palliative care referral to address negative associations and decrease patient fear of abandonment.

Focus Initial Palliative Care Referral on Symptom Management to Dissociate Palliative Care From End-of-Life Care and Facilitate Early Relationship Building With Palliative Care Clinicians

A majority of participants (20 of 34 participants) discussed using symptom management as the initial reason for referral to outpatient specialty palliative care to disassociate referral from end-of-life care (Table 3). As one participant described:

Table 3.

Representative Quotations Supporting Identified Strategies

I try to kind of disconnect hospice from palliative care, you know, and so I think she seemed open to talking with them, especially when I focused on the ways that they could try and help her with the symptoms that she was experiencing.

Physicians anticipated that referral for reasons associated with end-of-life or hospice care would cause distress in their patients and be met with resistance or refusal and felt that reframing the referral in the context of symptoms fostered acceptance: “She was fine with it because it wasn’t done in the context of ‘this is headed towards death’; it was done in the context of she has symptoms related to her cancer.” One participant explained how referring for symptom management facilitated both early referral and patient acceptance:

You get them involved before she starts to go down the drain so she doesn’t feel like these people are being introduced to have the death and dying talk with her…. A lot of these patients their only association with palliative care equates to hospice, and so if you can introduce them before you start having those kind of discussions, the focus can then be on what she wants moving forward, how we’re going to control her symptoms, and easing us into that conversation when the time comes

Referral for symptom management was also frequently identified as a mechanism to promote relationship building between palliative care clinicians and patients with poor prognoses. As one participant explained:

[There are] two benefits, there’s short term, and short term is better management of her symptoms that affect her quality of life, but long term, to have people around who she becomes familiar with so when we’re ready to have hospice she’s comfortable with the decision because these aren’t strangers to her.

This strategy was felt to facilitate earlier referral to palliative care and increase patient acceptance: “Earlier referral makes it not such a scary concept when you talk about it later; when the phases of care change, they’re already comfortable with that, so I think that’s one benefit.” Another participant explained how this approach enabled him to provide an improved quality of care:

The destiny for those patients after recurrence of fallopian or ovarian cancer is that as a rule they will ultimately die of that disease, so I like to get them involved early…so it’s an ongoing relationship that’s built over a period of time as opposed to the old practice of referring a patient to hospice care and they pass on within two to four weeks of a referral which is inferior care.

Use a Strong Oncologist-Patient Relationship and Patient Trust to Increase Acceptance of Referral

Many participants (16 of 34 participants) identified a strong relationship with their patients as key to patient acceptance of palliative care referral (Table 3). A strong oncologist-patient relationship was felt to facilitate open dialogue and allow the physician to tailor the timing and content of discussions about palliative care referral. One participant explained how the strength of her relationships with patients enabled her to more effectively initiate conversations about palliative care referral:

Because we do the long-term follow-up for our patients and we know them so well, I think it in many ways it just makes it easier to have very frank conversations with patients about things like involvement of palliative care.

In addition to aiding the initiation of conversations about palliative care referral, strong oncologist-patient relationships were felt to help oncologists individualize the discussion and lead to increased acceptance:

Different patients and different families have different reactions to the words palliative care, so I think that it is important to know your patient, have a sense of how they’re going to respond to that and I guess I would say frame it in the right way.

One participant discussed how the trust that develops from strong relationships promotes acceptance of referral:

I think you develop a trust with the patient and it’s just another thing that you’re recommending to them, and it’s not seen as out of the blue, it’s just part of the care…. I think if you’re comfortable and they trust you, they’re going to kind of accept and trust what you’re recommending.

A strong oncologist-patient relationship was also felt to increase acceptance of palliative care referral by allowing a longitudinal discussion. As one participant explained, “If they seem a little bit resistant, I kind of address the need; we bring it up, we talk about it, and I try to circle back to it in the subsequent visits.” The perceived value of a strong relationship in promoting acceptance was further illustrated by another participant who described waiting to make a palliative care referral until she developed a stronger relationship with her patients:

I might introduce the concept but not make the referral yet, just telling them that we work together, and it’s somebody that they’ll meet down the road, and then once we’ve established a treatment plan and they’ve met me, and started a relationship with me, then introducing it after a couple of visits.

Explain and Normalize Palliative Care Referral to Address Negative Associations and Decrease Patient Fear of Abandonment

Many participants (16 of 34 participants) emphasized the importance of explaining and normalizing palliative care to increase patient acceptance of referral (Table 3). Participants frequently attributed patient resistance to the association of the term palliative care with hospice. Participants felt that this association could be overcome by taking the time to clearly explain palliative care. As one participant explained:

I think that it’s all about the language. I can tell you, to the patient the word “palliative” is synonymous with hospice, is synonymous with “I’m dying and the doctor is now giving up” in the perception of the patient, but it depends on how it is introduced to them.

Another participant remarked:

I think the problem is that palliative care has a horrible name…because it just brings up a lot of negative connotations to people, rightly or wrongly. I think a lot of people think when you say palliative care they almost equate that to hospice and giving up, and so I think once you explain that it really is more about aggressive symptom management and enhancement of quality of life, but I think for the most part it always requires a little bit of effort to explain what palliative care does.

Patient fear of abandonment was also frequently discussed as a reason for resistance to referral, and participants felt that this also could be addressed with time and clear explanation. One participant explained how upfront discussion could prevent a patient from feeling abandoned:

I think there’s always the concern that the patient feels like you’re writing them off as a lost case, that you’re losing hope in them, and that you’re giving up on them, but if that is addressed at the outset and that discussion is hadand it’s not just “Here, go see these people” and it’s not introduced appropriately then it’s a problem, but as long as it’s introduced appropriately and the patient’s willing I feel like that usually can be avoided pretty easily.

Another participant discussed the importance of acknowledging and directly addressing this concern:

I think that any time you have somebody who has a new cancer recurrence and you’re referring them to a different group of providers, you just worry, or the patient might worry, does this mean that you can’t do anything else for me, does this mean that you’re giving up on me, does this mean that you’re just going to let me die, which you know certainly is not what it means when I refer people to palliative care, but feel like sometimes that needs to be very explicitly stated.

Participants also frequently discussed the value of normalizing palliative care referral to make it feel less threatening to patients: “I try to do that in an unobtrusive way by just making it kind of…what I do with all of my patients.” One participant discussed both normalizing palliative care referral and adjusting the wording used to describe the service: “So, palliative care is something you do in the office in the same way you would have her see her internist for her diabetes.… I don’t necessarily use the word palliative care; I use the term supportive care.” Another participant explained how normalizing palliative care as just an additional layer of care increased patient acceptance of referral: “I mean, sometimes, if you talk of palliative care as just another layer of support, which is the catch phrase that I like to use, I find that very very few patients recoil from that.”

DISCUSSION

Gynecologic oncologists at institutions with well-established palliative care services use a variety of strategies when presenting a palliative care referral to patients. These strategies aim to directly address the concern that patients may have negative associations with the idea of palliative care and thus may resist or decline referral.

Participants frequently focus initial palliative care referral on symptom management, even when symptoms are mild or there are additional reasons for referral such as discussion of goals of care or anticipated hospice needs. Symptom management is viewed as distinct from end-of-life issues, and this indication for referral may be less threatening to patients. When a patient accepts referral for symptom management, a relationship is developed with the palliative care team that promotes a smooth transition into end-of-life discussion and hospice should it be needed in the future. This is also an important strategy for situations in which the physician is uncomfortable or unwilling to discuss a poor prognosis. By providing an approach that can be used for patients with reservations about the full spectrum of palliative care services and by physicians without requiring a complete discussion of prognosis and goals, this strategy promotes physician adherence to national recommendations promoting the initiation of palliative care early in the disease course.

Gynecologic oncologists also use patient trust, which arises from strong oncologist-patient relationships, to increase acceptance of palliative care referral. Patients are more likely to pursue palliative care referral if it is recommended by their oncologist.²¹ The unique longitudinal nature of gynecologic oncology, with the oncologist providing care from diagnosis, through surgery and chemotherapy, and into surveillance or end-of-life care, may be particularly important to a patient accepting the recommendation of palliative care. Developing strong oncologist-patient relationships and using patient trust to encourage acceptance of palliative care referral are strategies that promotes the integration of palliative care into standard oncology care.

Another strategy for overcoming negative patient views of palliative care is through clear explanation of what palliative care encompasses and normalization of early referral. Negative associations with the term palliative care have been well documented among both physicians²² and patients.^23,24 There has been discussion about renaming palliative care; however, a recent study found that patients want a broader rebranding of palliative care and prefer an approach focusing on explanation, education, and incorporation into routine care.²⁵ Our study found that although physicians consider the possible negative connotations of the words palliative care and sometimes seek to use different terminology, they also believe that the most effective approach to addressing negative associations is through clear explanation and presenting referral as a routine part of care. This concordance between patients and physicians supports explanation and normalization as a promising strategy to facilitating acceptance of palliative care referral.

Strengths of our study include the large qualitative sample size and high response rate, as well as the inclusion of providers from multiple institutions with varying geography, size, and palliative care system structure. Because our study only included gynecologic oncologists at academic institutions with established outpatient palliative care clinics, our results may not be generalizable to medical, surgical, or radiation oncologists or to community practices or settings where palliative care is less available or less well established. Given that this study looks specifically at institutions with established palliative care access and integration, participants likely have an increased level of knowledge and awareness of palliative care services compared with gynecologic oncologists practicing in other settings and/or a predisposition to a positive view of palliative care integration into oncology. Although a positive bias toward palliative care may exist in the population surveyed, this provides an excellent starting point for discussion and for developing approaches to improving the integration of palliative care. In addition, the design of our study did not allow us to measure actual referral practices. A next step would be to directly assess the impact of these strategies on patient acceptance of palliative care referral and use of specialty palliative care services.

In summary, we found that gynecologic oncologists have specific strategies for introducing palliative care that proactively address negative patient associations and increase patient acceptance of referral. Strategies involve focusing initial referral on symptom management to encourage early relationship building and dissociate palliative care from end-of-life care, using trust built from strong oncologist-patient relationships, and normalizing and explaining palliative care services. These strategies provide groundwork for developing new approaches to improving the integration of palliative care into standard oncology care.

AUTHOR CONTRIBUTIONS

Conception and design: Casey M. Hay, Carolyn Lefkowits, Yael Schenker

Collection and assembly of data: Casey M. Hay, Marie A. Bakitas, Leslie H. Clark, Linda R. Duska, Renata R. Urban, Yael Schenker

Data analysis and interpretation: Casey M. Hay, Carolyn Lefkowits, Megan Crowley-Matoka, Marie A. Bakitas, Linda R. Duska, Stephanie L. Creasy, Yael Schenker

Manuscript writing: All authors

Final approval of manuscript: All authors

Accountable for all aspects of the work: All authors

AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

Strategies for Introducing Outpatient Specialty Palliative Care in Gynecologic Oncology

The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I = Immediate Family Member, Inst = My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO's conflict of interest policy, please refer to www.asco.org/rwc or ascopubs.org/journal/jop/site/misc/ifc.xhtml.

Casey M. Hay

No relationship to disclose

Carolyn Lefkowits

No relationship to disclose

Megan Crowley-Matoka

No relationship to disclose

Marie A. Bakitas

No relationship to disclose

Leslie H. Clark

No relationship to disclose

Linda R. Duska

Consulting or Advisory Role: Parexel, Advance Medical, Clearview Medical

Research Funding: Merck (Inst), Novartis (Inst), Pfizer (Inst), Tesaro (Inst), Abbott/AbbVie (Inst)

Renata R. Urban

No relationship to disclose

Stephanie L. Creasy

No relationship to disclose

Yael Schenker

No relationship to disclose